Combining GWAS and population genomic analyses to characterize coevolution in a legume-rhizobia symbiosis.
Medicago
bacteria
microbes
mutualism
population genomics
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
revised:
03
06
2022
received:
04
03
2022
accepted:
04
07
2022
medline:
11
7
2023
pubmed:
7
7
2022
entrez:
6
7
2022
Statut:
ppublish
Résumé
The mutualism between legumes and rhizobia is clearly the product of past coevolution. However, the nature of ongoing evolution between these partners is less clear. To characterize the nature of recent coevolution between legumes and rhizobia, we used population genomic analysis to characterize selection on functionally annotated symbiosis genes as well as on symbiosis gene candidates identified through a two-species association analysis. For the association analysis, we inoculated each of 202 accessions of the legume host Medicago truncatula with a community of 88 Sinorhizobia (Ensifer) meliloti strains. Multistrain inoculation, which better reflects the ecological reality of rhizobial selection in nature than single-strain inoculation, allows strains to compete for nodulation opportunities and host resources and for hosts to preferentially form nodules and provide resources to some strains. We found extensive host by symbiont, that is, genotype-by-genotype, effects on rhizobial fitness and some annotated rhizobial genes bear signatures of recent positive selection. However, neither genes responsible for this variation nor annotated host symbiosis genes are enriched for signatures of either positive or balancing selection. This result suggests that stabilizing selection dominates selection acting on symbiotic traits and that variation in these traits is under mutation-selection balance. Consistent with the lack of positive selection acting on host genes, we found that among-host variation in growth was similar whether plants were grown with rhizobia or N-fertilizer, suggesting that the symbiosis may not be a major driver of variation in plant growth in multistrain contexts.
Banques de données
RefSeq
['GCA_003473485.1', 'Medtr5g094210', 'Medtr7g063220', 'Medtr7g078700', 'Medtr8g067470', 'Medtr8g465280', 'MT35v5_contig_51603_1', 'MT35v5_contig_52215_1', 'MT35v5_contig_55897_1', 'MT4Noble_057132', 'Medtr1g027020', 'Medtr4g073400', 'Medtr5g007630', 'Medtr5g026460']
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
3798-3811Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.
Références
Abney, M. (2015). Permutation testing in the presence of polygenic variation. Genetic Epidemiology, 39(4), 249-258. https://doi.org/10.1002/gepi.21893
Alachiotis, N., & Pavlidis, P. (2018). RAiSD detects positive selection based on multiple signatures of a selective sweep and SNP vectors. Communications Biology, 1(1), 79. https://doi.org/10.1038/s42003-018-0085-8
Atwell, S., Huang, Y. S., Vilhjálmsson, B. J., Willems, G., Horton, M., Li, Y., Meng, D., Platt, A., Tarone, A. M., Hu, T. T., Jiang, R., Muliyati, N. W., Zhang, X., Amer, M. A., Baxter, I., Brachi, B., Chory, J., Dean, C., Debieu, M., … Nordborg, M. (2010). Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature, 465, 627-631.
Baev, N., Schultze, M., Barlier, I., Ha, D. C., Virelizier, H., Kondorosi, E., & Kondorosi, A. (1992). Rhizobium nodM and nodN genes are common nod genes: NodM encodes functions for efficiency of nod signal production and bacteroid maturation. Journal of Bacteriology, 174(23), 7555-7565. https://doi.org/10.1128/jb.174.23.7555-7565.1992
Bailly, X., Olivieri, I., De Mita, S., Cleyet-Marel, J.-C., & Béna, G. (2006). Recombination and selection shape the molecular diversity pattern of nitrogen-fixing Sinorhizobium sp. associated to Medicago. Molecular Ecology, 15(10), 2719-2734. https://doi.org/10.1111/j.1365-294X.2006.02969.x
Bálint, M., Bartha, L., O'Hara, R. B., Olson, M. S., Otte, J., Pfenninger, M., Robertson, A. L., Tiffin, P., & Schmitt, I. (2015). Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars. Molecular Ecology, 24(1), 235-248. https://doi.org/10.1111/mec.13018
Bamba, M., Aoki, S., Kajita, T., Setoguchi, H., Watano, Y., Sato, S., & Tsuchimatsu, T. (2020). Massive rhizobial genomic variation associated with partner quality in Lotus-Mesorhizobium symbiosis. FEMS Microbiology Ecology, 96(12), fiaa202. https://doi.org/10.1093/femsec/fiaa202
Batstone, R. T., Burghardt, L. T., & Heath, K. D. (2021). The genetic basis of cooperation and conflict in natural populations of a model symbiont. BioRxiv. https://doi.org/10.1101/2021.07.19.452989
Batstone, R. T., O'Brien, A. M., Harrison, T. L., & Frederickson, M. E. (2020). Experimental evolution makes microbes more cooperative with their local host genotype. Science, 370(6515), 476-478.
Bever, J. D. (2002). Dynamics within mutualism and the maintenance of diversity: Inference from a model of interguild frequency dependence. Ecology Letters, 2(1), 52-61. https://doi.org/10.1046/j.1461-0248.1999.21050.x
Bohlool, B. B., & Schmidt, E. L. (1974). Lectins: A possible basis for specificity in the rhizobium-Legume root nodule symbiosis. Science, 185(4147), 269-271. https://doi.org/10.1126/science.185.4147.269
Bonhomme, M., Boitard, S., San Clemente, H., Dumas, B., Young, N., & Jacquet, C. (2015). Genomic signature of selective sweeps illuminates adaptation of Medicago truncatula to root-associated microorganisms. Molecular Biology and Evolution, 32(8), 2097-2110. https://doi.org/10.1093/molbev/msv092
Branca, A., Paape, T. D., Zhou, P., Briskine, R., Farmer, A. D., Mudge, J., Bharti, A. K., Woodward, J. E., May, G. D., Gentzbittel, L., Ben, C., Denny, R., Sadowsky, M. J., Ronfort, J., Bataillon, T., Young, N. D., & Tiffin, P. (2011). Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proceedings of the National Academy of Sciences, 108(42), E864-E870. https://doi.org/10.1073/pnas.1104032108
Bulik-Sullivan, B. K., Loh, P.-R., Finucane, H. K., Ripke, S., Yang, J., Schizophrenia Working Group of the Psychiatric Genomics Consortium, Patterson, N., Daly, M. J., Price, A. L., & Neale, B. M. (2015). LD Score regression distinguishes confounding from polygenicity in genome-wide association studies. Nature Genetics, 47(3), 291-295.
Burdon, J. J., Gibson, A. H., Searle, S. D., Woods, M. J., & Brockwell, J. (1999). Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian Acacia: Within-species interactions. Journal of Applied Ecology, 36(3), 398-408. https://doi.org/10.1046/j.1365-2664.1999.00409.x
Burghardt, L. T., Epstein, B., Guhlin, J., Nelson, M. S., Taylor, M. R., Young, N. D., Sadowsky, M. J., & Tiffin, P. (2018). Select and resequence reveals relative fitness of bacteria in symbiotic and free-living environments. Proceedings of the National Academy of Sciences, 115(10), 2425-2430. https://doi.org/10.1073/pnas.1714246115
Burghardt, L. T., Epstein, B., & Tiffin, P. (2019). Legacy of prior host and soil selection on rhizobial fitness in planta. Evolution, 73, 2013-2023.
Chevin, L.-M., & Hospital, F. (2008). Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics, 180(3), 1645-1660. https://doi.org/10.1534/genetics.108.093351
De Mita, S., Ronfort, J., McKhann, H. I., Poncet, C., El Malki, R., & Bataillon, T. (2007). Investigation of the demographic and selective forces shaping the nucleotide diversity of genes involved in nod factor signaling in Medicago truncatula. Genetics, 177(4), 2123-2133. https://doi.org/10.1534/genetics.107.076943
De Mita, S., Santoni, S., Hochu, I., Ronfort, J., & Bataillon, T. (2006). Molecular evolution and positive selection of the symbiotic gene NORK in Medicago truncatula. Journal of Molecular Evolution, 62(2), 234-244. https://doi.org/10.1007/s00239-004-0367-2
Delgado, M. J., Bedmar, E. J., & Downie, J. A. (1998). Genes involved in the formation and assembly of rhizobial cytochromes and their role in symbiotic nitrogen fixation. In R. K. Poole (Ed.), Advances in microbial physiology (pp. 191-231). Academic Press. https://doi.org/10.1016/S0065-2911(08)60132-0
Denison, R. F., & Kiers, E. T. (2011). Life histories of symbiotic rhizobia and mycorrhizal fungi. Current Biology, 21(18), R775-R785. https://doi.org/10.1016/j.cub.2011.06.018
Doyle, J. J. (1998). Phylogenetic perspectives on nodulation: Evolving views of plants and symbiotic bacteria. Trends in Plant Science, 3(12), 473-478. https://doi.org/10.1016/S1360-1385(98)01340-5
Ebert, D., & Fields, P. D. (2020). Host-parasite co-evolution and its genomic signature. Nature Reviews Genetics, 21, 754-768.
Epstein, B., Abou-Shanab, R. A. I., Shamseldin, A., Taylor, M. R., Guhlin, J., Burghardt, L. T., Nelson, M., Sadowsky, M. J., & Tiffin, P. (2018). Genome-wide association analyses in the model rhizobium Ensifer meliloti. MSphere, 3(5), e00386-e00318. https://doi.org/10.1128/mSphere.00386-18
Epstein, B., Branca, A., Mudge, J., Bharti, A. K., Briskine, R., Farmer, A. D., Sugawara, M., Young, N. D., Sadowsky, M. J., & Tiffin, P. (2012). Population genomics of the facultatively mutualistic bacteria Sinorhizobium meliloti and S. medicae. PLoS Genetics, 8(8), e1002868. https://doi.org/10.1371/journal.pgen.1002868
Epstein, B., & Tiffin, P. (2021). Comparative genomics reveals high rates of horizontal transfer and strong purifying selection on rhizobial symbiosis genes. Proceedings of the Royal Society B, 288(1942), 20201804.
Eswaramoorthy, S., Bonanno, J. B., Burley, S. K., & Swaminathan, S. (2006). Mechanism of action of a flavin-containing monooxygenase. Proceedings of the National Academy of Sciences, 103(26), 9832-9837. https://doi.org/10.1073/pnas.0602398103
Fiebig, A., Castro Rojas, C. M., Siegal-Gaskins, D., & Crosson, S. (2010). Interaction specificity, toxicity and regulation of a paralogous set of ParE/RelE-family toxin-antitoxin systems. Molecular Microbiology, 77(1), 236-251. https://doi.org/10.1111/j.1365-2958.2010.07207.x
Frederickson, M. E. (2013). Rethinking mutualism stability: Cheaters and the evolution of sanctions. The Quarterly Review of Biology, 88(4), 269-295. https://doi.org/10.1086/673757
Frederickson, M. E. (2017). Mutualisms are not on the verge of breakdown. Trends in Ecology & Evolution, 32(10), 727-734. https://doi.org/10.1016/j.tree.2017.07.001
Friesen, M. L. (2012). Widespread fitness alignment in the legume-rhizobium symbiosis. New Phytologist, 194(4), 1096-1111. https://doi.org/10.1111/j.1469-8137.2012.04099.x
Fullner, K. J., Stephens, K. M., & Nester, E. W. (1994). An essential virulence protein of Agrobacterium tumefaciens, VirB4, requires an intact mononucleotide binding domain to function in transfer of T-DNA. Molecular & general genetics, 245, 704-715.
Gano-Cohen, K. A., Wendlandt, C. E., Al Moussawi, K., Stokes, P. J., Quides, K. W., Weisberg, A. J., Chang, J. H., & Sachs, J. L. (2020). Recurrent mutualism breakdown events in a legume rhizobia metapopulation. Proceedings of the Royal Society B: Biological Sciences, 287(1919), 20192549. https://doi.org/10.1098/rspb.2019.2549
Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., … Ley, R. E. (2014). Human genetics shape the gut microbiome. Cell, 159(4), 789-799. https://doi.org/10.1016/j.cell.2014.09.053
Grillo, M. A., De Mita, S., Burke, P. V., Solórzano-Lowell, K. L. S., & Heath, K. D. (2016). Intrapopulation genomics in a model mutualist: Population structure and candidate symbiosis genes under selection in Medicago truncatula. Evolution, 70(12), 2704-2717. https://doi.org/10.1111/evo.13095
Heath, K. D. (2010). Intergenomic epistasis and coevolutionary constraint in plants and rhizobia. Evolution, 64(5), 1446-1458. https://doi.org/10.1111/j.1558-5646.2009.00913.x
Heath, K. D., & Nuismer, S. L. (2014). Connecting functional and statistical definitions of genotype by genotype interactions in coevolutionary studies. Frontiers in Genetics, 5, 77. https://doi.org/10.3389/fgene.2014.00077
Heath, K. D., & Stinchcombe, J. R. (2014). Explaining mutualism variation: A new evolutionary paradox? Evolution, 68(2), 309-317.
Heath, K. D., & Tiffin, P. (2009). Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution, 63(3), 652-662. https://doi.org/10.1111/j.1558-5646.2008.00582.x
Hoeksema, J. D. (2010). Ongoing coevolution in mycorrhizal interactions. New Phytologist, 187(2), 286-300. https://doi.org/10.1111/j.1469-8137.2010.03305.x
Josephs, E. B., Stinchcombe, J. R., & Wright, S. I. (2017). What can genome-wide association studies tell us about the evolutionary forces maintaining genetic variation for quantitative traits? New Phytologist, 214(1), 21-33.
Kanamori, N., Madsen, L. H., Radutoiu, S., Frantescu, M., Quistgaard, E. M. H., Miwa, H., Downie, J. A., James, E. K., Felle, H. H., Haaning, L. L., Jensen, T. H., Sato, S., Nakamura, Y., Tabata, S., Sandal, N., & Stougaard, J. (2006). A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proceedings of the National Academy of Sciences, 103(2), 359-364. https://doi.org/10.1073/pnas.0508883103
Kessner, D., Turner, T. L., & Novembre, J. (2013). Maximum likelihood estimation of frequencies of known haplotypes from pooled sequence data. Molecular Biology and Evolution, 30(5), 1145-1158. https://doi.org/10.1093/molbev/mst016
Kiester, A. R., Lande, R., & Schemski, D. W. (1984). Models of coevolution and speciation in plants and their pollinators. American Naturalist, 124, 220-243.
Klinger, C. R., Lau, J. A., & Heath, K. D. (2016). Ecological genomics of mutualism decline in nitrogen-fixing bacteria. Proceedings of the Royal Society B: Biological Sciences, 283(1826), 20152563. https://doi.org/10.1098/rspb.2015.2563
Lindström, K., & Mousavi, S. A. (2020). Effectiveness of nitrogen fixation in rhizobia. Microbial Biotechnology, 13(5), 1314-1335. https://doi.org/10.1111/1751-7915.13517
MacPherson, A., Otto, S. P., & Nuismer, S. L. (2018). Keeping pace with the red queen: Identifying the genetic basis of susceptibility to infectious disease. Genetics, 208(2), 779-789. https://doi.org/10.1534/genetics.117.300481
Masson-Boivin, C., & Sachs, J. L. (2018). Symbiotic nitrogen fixation by rhizobia-The roots of a success story. Biotic Interactions, 44, 7-15. https://doi.org/10.1016/j.pbi.2017.12.001
Mendoza-Suárez, M. A., Geddes, B. A., Sánchez-Cañizares, C., Ramírez-González, R. H., Kirchhelle, C., Jorrin, B., & Poole, P. S. (2020). Optimizing Rhizobium-legume symbioses by simultaneous measurement of rhizobial competitiveness and N2 fixation in nodules. Proceedings of the National Academy of Sciences, 117(18), 9822-9831. https://doi.org/10.1073/pnas.1921225117
Myles, S., Peiffer, J., Brown, P. J., Ersoz, E. S., Zhang, Z., Costich, D. E., & Buckler, E. S. (2009). Association mapping: Critical considerations shift from genotyping to experimental design. The Plant Cell, 21(8), 2194-2202. https://doi.org/10.1105/tpc.109.068437
Nelson, M., Guhlin, J., Epstein, B., Tiffin, P., & Sadowsky, M. J. (2018). The complete replicons of 16 Ensifer meliloti strains offer insights into intra-and inter-replicon gene transfer, transposon-associated loci, and repeat elements. Microbial Genomics, 4(5), e000174.
Nelson, M. S., Chun, C. L., & Sadowsky, M. J. (2017). Type IV effector proteins involved in the Medicago-Sinorhizobium symbiosis. Molecular Plant-Microbe Interactions, 30(1), 28-34. https://doi.org/10.1094/MPMI-10-16-0211-R
Oono, R., Anderson, C. G., & Denison, R. F. (2011). Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proceedings of the Royal Society B: Biological Sciences, 278(1718), 2698-2703. https://doi.org/10.1098/rspb.2010.2193
Ossler, J. N., & Heath, K. D. (2018). Shared genes but not shared genetic variation: legume colonization by two belowground symbionts. The American Naturalist, 191(3), 395-406. https://doi.org/10.1086/695829
Ostrowski, E. A., Shen, Y., Tian, X., Sucgang, R., Jiang, H., Qu, J., Katoh-Kurasawa, M., Brock, D. A., Dinh, C., Lara-Garduno, F., Lee, S. L., Kovar, C. L., Dinh, H. H., Korchina, V., Jackson, L., Patil, S., Han, Y., Chaboub, L., Shaulsky, G., … Queller, D. C. (2015). Genomic signatures of cooperation and conflict in the social amoeba. Current Biology, 25(12), 1661-1665. https://doi.org/10.1016/j.cub.2015.04.059
Paape, T., Bataillon, T., Zhou, P., Kono, T, J. Y., Briskine, R., Young, N. D., & Tiffin, P. (2013). Selection, genome-wide fitness effects and evolutionary rates in the model legume Medicago truncatula. Molecular Ecology, 22(13), 3525-3538. https://doi.org/10.1111/mec.12329
Parker, M. A. (1999). Mutualism in metapopulations of legumes and rhizobia. The American Naturalist, 153(S5), S48-S60. https://doi.org/10.1086/303211
Parker, M. P. (1995). Plant fitness variation caused by different mutualist genotypes. Ecology, 76(5), 1525-1535. https://doi.org/10.2307/1938154
Pecrix, Y., Staton, S. E., Sallet, E., Lelandais-Brière, C., Moreau, S., Carrère, S., Blein, T., Jardinaud, M., Latrsse, D., Zouine, M., Zahm, M., Chantry-Darmon, C., Lopez-Roquest, C., Bouchez, O., Bérard, A., Debelle, F., Muños, S., Bendahmane, A., Bergès, H., … Gamas, P. (2018). Whole-genome landscape of Medicago truncatula symbiotic genes. Nature Plants, 4(12), 1017-1025. https://doi.org/10.1038/s41477-018-0286-7
Porter, S. S., & Simms, E. L. (2014). Selection for cheating across disparate environments in the legume-rhizobium mutualism. Ecology Letters, 17(9), 1121-1129. https://doi.org/10.1111/ele.12318
Pritchard, J. K., Pickrell, J. K., & Coop, G. (2010). The Genetics of Human Adaptation: Hard Sweeps, Soft Sweeps, and Polygenic Adaptation. Current Biology, 20(4), R208-R215. https://doi.org/10.1016/j.cub.2009.11.055
Queller, D. C., & Strassmann, J. E. (2018). Evolutionary Conflict. Annual Review of Ecology, Evolution, and Systematics, 49(1), 73-93. https://doi.org/10.1146/annurev-ecolsys-110617-062527
Quides, K. W., Weisberg, A. J., Trinh, J., Salaheldine, F., Cardenas, P., Lee, H.-H., Jariwata, R., Chang, J. H., & Sachs, J. L. (2021). Experimental evolution can enhance benefits of rhizobia to novel legume hosts. Proceedings of the Royal Society B: Biological Sciences, 288(1951), 20210812. https://doi.org/10.1098/rspb.2021.0812
Rangin, C., Brunel, B., Cleyet-Marel, J.-C., Perrineau, M.-M., & Béna, G. (2008). Effects of Medicago truncatula genetic diversity, rhizobial competition, and strain effectiveness on the diversity of a natural Sinorhizobium species community. Applied and Environmental Microbiology, 74(18), 5653-5661.
Ratcliff, W. C., Underbakke, K., & Denison, R. F. (2011). Measuring the fitness of symbiotic rhizobia. Symbiosis, 55(2), 85-90. https://doi.org/10.1007/s13199-011-0150-2
Regus, J. U., Quides, K. W., O'Neill, M. R., Suzuki, R., Savory, E. A., Chang, J. H., & Sachs, J. L. (2017). Cell autonomous sanctions in legumes target ineffective rhizobia in nodules with mixed infections. American Journal of Botany, 104(9), 1299-1312. https://doi.org/10.3732/ajb.1700165
Riley, A., Grillo, M., Epstein, B., Tiffin, P., & Heath, K. D. (2022). Discordant population structure within rhizobium divided genomes and between rhizobia and legume hosts in their native range. Authorea. https://doi.org/10.22541/au.164637769.91740255/v1
Roy, S., Liu, W., Nandety, R. S., Crook, A., Mysore, K. S., Pislariu, C. I., Frugoli, J., Dickstein, R., & Udvardi, M. K. (2020). Celebrating 20 Years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. The Plant Cell, 32(1), 15-41. https://doi.org/10.1105/tpc.19.00279
Rutten, P. J. H., Steel, G. A., Hood, V. K., Ramachandran, L., McMurtry, B., Geddes, B., Papachristodoulou, A., & Poole, P. S. (2021). Multiple sensors provide spatiotemporal oxygen regulation of gene expression in a Rhizobium-legume symbiosis. PLoS Genetics., 17, e1009099. https://doi.org/10.1371/journal.pgen.1009099
Ruvkun, G. B., Sundaresan, V., & Ausubel, F. M. (1982). Directed transposon Tn5 mutagenesis and complementation analysis of rhizobium meliloti symbiotic nitrogen fixation genes. Cell, 29(2), 551-559. https://doi.org/10.1016/0092-8674(82)90171-4
Sachs, J. L., Essenberg, C. J., & Turcotte, M. M. (2011). New paradigms for the evolution of beneficial infections. Trends in Ecology & Evolution, 26(4), 202-209. https://doi.org/10.1016/j.tree.2011.01.010
Sachs, J. L., Quides, K. W., & Wendlandt, C. E. (2018). Legumes versus rhizobia: A model for ongoing conflict in symbiosis. New Phytologist, 219(4), 1199-1206. https://doi.org/10.1111/nph.15222
Saturno, D. F., Cerezini, P., Moreira da Silva, P., Oliveira, A. B., Oliveira, M. C. N., Hungria, M., & Nogueira, M. A. (2017). Mineral nitrogen impairs the biological nitrogen fixation in soybean of determinate and indeterminate growth types. Journal of Plant Nutrition, 40(12), 1690-1701. https://doi.org/10.1080/01904167.2017.1310890
Siewert, K. M., & Voight, B. F. (2020). BetaScan2: Standardized statistics to detect balancing selection utilizing substitution data. Genome Biology and Evolution, 12(2), 3873-3877. https://doi.org/10.1093/gbe/evaa013
Simonsen, A. K., & Stinchcombe, J. R. (2014). Standing genetic variation in host preference for mutualist microbial symbionts. Proceedings of the Royal Society B: Biological Sciences, 281(1797), 20142036. https://doi.org/10.1098/rspb.2014.2036
Somasegaran, P., & Bohlool, B. B. (1990). Single-strain versus multistrain inoculation: effect of soil mineral n availability on rhizobial strain effectiveness and competition for nodulation on chick-pea, soybean, and dry bean. Applied and Environmental Microbiology, 56(11), 3298-3303. https://doi.org/10.1128/aem.56.11.3298-3303.1990
Sprent, J. I. (2008). 60Ma of legume nodulation. What's new? What's changing? Journal of Experimental Botany, 59(5), 1081-1084. https://doi.org/10.1093/jxb/erm286
Stanton-Geddes, J., Paape, T., Epstein, B., Briskine, R., Yoder, J., Mudge, J., Bharti, A. K., Farmer, A. D., Zhou, P., Cenny, R., May, G. D., Erlandson, S., Yakub, M., Sugawara, M., Sadkowsky, M. J., Young, N. D., & Tiffin, P. (2013). Candidate genes and genetic architecture of symbiotic and agronomic traits revealed by whole-genome, sequence-based association genetics in Medicago truncatula. PLoS One, 8(5), e65688. https://doi.org/10.1371/journal.pone.0065688
Sugawara, M., Epstein, B., Badgley, B. D., Unno, T., Xu, L., Reese, J., Gyaneshwar, P., Denny, R., Mudge, J., Bharti, A. K., Parmer, A. D., May, G. D., Woodward, J. E., Médigue, C.,Vallenet, D., Laius, A. l., Rouy, Z., Martinez-Vaz, B., Tiffin, P., … Sadwosky, M. J. (2013). Comparative genomics of the core and accessory genomes of 48 Sinorhizobium strains comprising five genospecies. Genome Biology, 14(2), R17.
Thrall, P. H., Hochberg, M. E., Burdon, J. J., & Bever, J. D. (2007). Coevolution of symbiotic mutualists and parasites in a community context. Trends in Ecology & Evolution, 22(3), 120-126. https://doi.org/10.1016/j.tree.2006.11.007
Torkamaneh, D., Chalifour, F.-P., Beauchamp, C. J., Agrama, H., Boahen, S., Maaroufi, H., Rajcan, I., & Belzile, F. (2020). Genome-wide association analyses reveal the genetic basis of biomass accumulation under symbiotic nitrogen fixation in African soybean. Theoretical and Applied Genetics, 133(2), 665-676. https://doi.org/10.1007/s00122-019-03499-7
Veyron, S., Peyroche, G., & Cherfils, J. (2018). FIC proteins: From bacteria to humans and back again. Pathogens and Disease, 76(2), fty012. https://doi.org/10.1093/femspd/fty012
Voichek, Y., & Weigel, D. (2020). Identifying genetic variants underlying phenotypic variation in plants without complete genomes. Nature Genetics, 52(5), 534-540. https://doi.org/10.1038/s41588-020-0612-7
Wade, M. J. (2007). The co-evolutionary genetics of ecological communities. Nature Reviews Genetics, 8(3), 185-195. https://doi.org/10.1038/nrg2031
Wang, D., Yang, S., Tang, F., & Zhu, H. (2012). Symbiosis specificity in the legume - rhizobial mutualism. Cellular Microbiology, 14(3), 334-342. https://doi.org/10.1111/j.1462-5822.2011.01736.x
Weese, D. J., Heath, K. D., Dentinger, B. T. M., & Lau, J. A. (2015). Long-term nitrogen addition causes the evolution of less-cooperative mutualists. Evolution, 69(3), 631-642. https://doi.org/10.1111/evo.12594
Wendlandt, C. E., Helliwell, E., Roberts, M., Nguyen, K. T., Friesen, M. L., von Wettberg, E., Price, P., Griffitts, J. S., & Porter, S. S. (2021). Decreased coevolutionary potential and increased symbiont fecundity during the biological invasion of a legume-rhizobium mutualism. Evolution, 75(3), 731-747. https://doi.org/10.1111/evo.14164
Wendlandt, C. E., Regus, J. U., Gano-Cohen, K. A., Hollowell, A. C., Quides, K. W., Lyu, J. Y., Adinata, E. S., & Sachs, J. L. (2019). Host investment into symbiosis varies among genotypes of the legume Acmispon strigosus, but host sanctions are uniform. New Phytologist, 221(1), 446-458. https://doi.org/10.1111/nph.15378
West, S. A., Kiers, E. T., Simms, E. L., & Denison, R. F. (2002). Sanctions and mutualism stability: Why do rhizobia fix nitrogen? Proceedings of the Royal Society of London. Series B: Biological Sciences, 269(1492), 685-694. https://doi.org/10.1098/rspb.2001.1878
Yoder, J. B. (2016). Understanding the coevolutionary dynamics of mutualism with population genomics. American Journal of Botany, 103(10), 1742-1752. https://doi.org/10.3732/ajb.1600154
Young, J. P. W., & Johnston, A. W. B. (1989). The evolution of specificity in the legume-rhizobium symbiosis. Trends in Ecology & Evolution, 4(11), 341-349. https://doi.org/10.1016/0169-5347(89)90089-X
Zhao, Y., Huang, J., Wang, Z., Jing, S., Wang, Y., Ouyang, Y., Cai, B., Zin, X-F., Lieu, X., Zhang, C., Pan, Y., Ma, R., Li, O., Jiang, W., Zeng, Y., Shangguan, X., Wang, H., Du, B., Zhu, L., … He, G. (2016). Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation. Proceedings of the National Academy of Sciences, 113(45), 12850-12855. https://doi.org/10.1073/pnas.1614862113
Zhou, X., & Stephens, M. (2012). Genome-wide efficient mixed-model analysis for association studies. Nature Genetics, 44(7), 821-824.